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Occurrence of Imposex in Thais Haemastoma: Possible Evidence of Environmental Contamination Derived from Organotin Compounds in Rio De Janeiro and Fortaleza, Brazil

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Occurrence of Imposex in Thais Haemastoma: Possible Evidence of Environmental Contamination Derived from Organotin Compounds in Rio De Janeiro and Fortaleza, Brazil ARTIGO ARTICLE 463 Occurrence of imposex in Thais haemastoma: possible evidence of environmental contamination derived from organotin compounds in Rio de Janeiro and Fortaleza, Brazil Ocorrência de imposex em Thais haemastoma: Marcos Antonio Fernandez 1,2 possíveis evidências de contaminação ambiental Aricelso Maia Limaverde 1 por compostos organotínicos no Rio de Janeiro Italo Braga de Castro 3 e em Fortaleza, Brasil Ana Cristina Martins Almeida 1 Angela de Luca Rebello Wagener 1 1 Departamento de Química, Abstract There are indications that the widespread use of organotin compounds (TBT and TPT) Pontifícia Universidade as antifoulings, as stabilizers in plastic and as pesticides, has severely affected several species of Católica do Rio de Janeiro. Rua Marquês de São Vicente marine organisms. The most striking effect of TBT and TPT as hormonal disruptors is the devel- 225, Rio de Janeiro, RJ opment of male organs in females of gastropods, currently denominated imposex. This syndrome 22453-900, Brasil. can lead to the sterilization and death of affected organisms. The present work gives an overview 2 Departamento de Oceanografia, Universidade of the present state of knowledge on imposex occurrence and reports results of a survey conduct- do Estado do Rio de Janeiro. ed in Guanabara Bay, Rio de Janeiro and in several sites along the coast of Fortaleza, Ceará State. Rua São Francisco Xavier Different stages of imposex development were verified in this survey, however, the most promi- 524, sala 4018E, Rio de Janeiro, RJ nent levels appeared associated to known spot sources of TBT and TPT. 20550-013, Brasil. Key words Organotin Compounds; Thais haemastoma; Imposex; Endocrine Disruptors [email protected] 3 Departamento de Biologia, Laboratório de Malacologia, Resumo Existem evidências de que a utilização amplamente disseminada de compostos orga- Universidade Federal noestânicos (TBT e TPT) como antiincrustantes, estabilizadores em plásticos e como pesticidas do Ceará. Av. Humberto Monte s/n, Campus do Pici, tenha afetado severamente diversas espécies de organismos marinhos. O mais característico Bloco 909, Fortaleza, CE efeito do TBT e do TPT como desreguladores endócrinos é o desenvolvimento de caracteres sexuais 60000-000, Brasil. masculinos em fêmeas de gastrópodos, conhecido como imposex. Esta síndrome pode levar à es- terelização e morte dos organismos afetados. O presente trabalho apresenta uma vista geral ao estado atual do conhecimento sobre a ocorrência do imposex, e reporta os resultados de um es- tudo conduzido na Baía de Guanabara, Rio de Janeiro, e ao longo da costa de Fortaleza, no Ceará. Diferentes estágios de desenvolvimento do imposex foram verificados neste estudo, os mais proeminentes parecendo associados às fontes pontuais locais conhecidas de TBT e TPT. Palavras-chave Compostos Orgânicos de Estanho; Thais haemastoma; Imposex; Desregulado- res Endócrinos Cad. Saúde Pública, Rio de Janeiro, 18(2):463-476, mar-abr, 2002 464 FERNANDEZ, M. A. et al. Introduction the International Maritime Organization (IMO) recommended the global banning of organotin Organotin compounds have been in use since compounds as antifoulings by 2008 and the the 1960s. Due to its powerful antifouling effect prohibition of new application in boats by 2003 tributyltin (TBT) has been utilized as an addi- (Champ, 1999; ten Hallers-Tjabbes, 1997). In tive in paintings applied to ships, fishing nets, Brazil, however, there is no legislation impos- marine installations and cooling systems based ing restriction or addressing permissible levels, on seawater (Bacci & Gaggi, 1989; Fent, 1996; and up to very recently no investigations have Horiguchi et al., 1994; Short & Thrower, 1986). been conducted to evaluate possible environ- Triphenyltin (TPT) has been used in associa- mental impacts. tion with TBT in antifouling paintings but is al- By the beginning of the last decade, restric- so effectively applied as acaricide and fungi- tions imposed to the use of TBT and TPT in de- cide in agriculture and for wood preservation veloped countries had led to the decrease in (Favoreto, 2000; Fent, 1996; Mensink et al., concentration of the parent compounds and 1997). Di-substituted organotin compounds are decay products, both in waters and organisms. used as plastic stabilizers in PVC production Recoveries were observed in oyster popula- and as catalysts in some industrial processes. tions of Basin d’Arcachon (Alzieu, 1986) and in Environmental problems derived from the gastropods from coastal environments in Unit- use of organotin compounds as antifouling ed Kingdom (Evans et al., 1996; Tester et al., agents were first reported by the end of the 1996; Tester & Ellis, 1995). However, Kure & De- 1970s after a sharp decline in oyster produc- pledge (1994) reported that in Denmark, high tion was observed in the Basin d’Arcachon, concentrations could still be observed in filter France (Alzieu et al., 1986, 1989). The main bio- feeders years after establishment of the re- logical alterations initially ascribed to the wide- stricted use. spread use of organotins were balling in oysters Although TBT and TPT can be decomposed (Alzieu et al., 1986, 1989; Axiak et al., 1995; in the water column rather fast (half life time ~ Dyrinda, 1992), death of mollusk larvae (Hori- 7-15 days) (Foale, 1993), estimated half life of gushi et al., 1998) and imposition of male sexu- the order of 1 year for toxic sediments, to al characteristics to females of gastropods (El- decades for anoxic sediments, are indicative of lis & Pattisina, 1990; Fioroni et al., 1991; Gibbs relatively high persistence in these environ- & Bryan, 1987). This last effect, denominated ments, specially in the absence of oxygen (Dow- imposex is induced in several gastropod species son et al., 1996). In environments with high both in the field and in laboratory studies at particulate loads where photochemical reac- very low concentrations of TBT (imposex is ini- tions are less active and transport to sediments tiated at less than 1ng/L-1 TBT in Nucella la- may occur before extensive degradation in the pilus, and at 3-5ng/L-1 all females may be ster- water column takes place, sediments are a po- ilized (Gibbs & Bryan, 1994; concentrations of tential source of TBT and TPT even after the 1ng/L-1 can induce imposex development in use has been interrupted (Dowson et al., 1993, Thais clavigera, Horiguchi et al., 1995). This wide- 1996; Langston & Pope, 1995; Sarradin et al., ly observed effects suggests that TBT and TPT 1991, 1994). The tendency to accumulate in may also act as endocrinal disruptors (Horiguchi sediments becomes evident from the levels of et al., 1995, 1997a; Liu & Suen, 1996; Math- TBT reported for contaminated sediments that iessen & Gibbs, 1998; Oehlmann et al., 1996). may range from 300ng.g-1 up to 1,000ng.g-1 or The detrimental effects of TBT and TPT up- more, when compared to slightly contaminat- on non-target organisms led to restrictions to ed sediments, where levels are in the range of the use, first in France in 1982, where antifoul- 10 to 50ng.g-1 (Waite et al., 1991). Values as high ing paintings containing TBT were prohibited as 4,500ng.g-1 TBT in sediments where detect- for boats of less than 25m length (Sarradin et al., ed in Thailand (Kan-Atireklap et al., 1997a) or 1991; Waite et al., 1991), and then in many other 3,200ng.g-1 TBT in Hong-Kong (Ko et al., 1995). countries, such as the United Kingdom (1987), After 1994, reports from several authors on United States (1988), Sweden, New Zealand the presence of TBT in higher organisms in- (1989), Australia, Japan (1990) and Denmark cluding cetaceans (Iwata et al., 1994; Kannan & (1991) (Champ & Pugh, 1987; de Mora et al., Falandysz, 1997; Tanabe, 1999), marine birds 1989; Horiguchi et al., 1994; Kure & Depledge, (Guruge et al., 1997a, 1997b) and humans (Kan- 1994; May et al., 1993; Stewart & de Mora, 1990; nan & Falandysz, 1997; Takahashi et al., 1999) Stuer-Lauridsen & Dahl, 1995). Germany and demonstrated that organotin compounds are Switzerland imposed restrictions also for fresh- likely to be transferred among different trophic water environments (Champ, 1986). Recently levels. Cad. Saúde Pública, Rio de Janeiro, 18(2):463-476, mar-abr, 2002 POSSIBLE EVIDENCE OF ENVIRONMENTAL CONTAMINATION BY ORGANOTIN COMPOUNDS 465 Little is known about the behavior of organ- al., 1997) and invertebrates (mollusks and tuni- otin compounds in tropical marine environ- cates) (Cima et al., 1995; Morcillo & Porte, ments. Imposex has been observed in several 1997) call for epidemiological investigations species of gastropod on the coast of India (Cro- focused upon sensitive populations. nia konkanensis – Vishwa-Kiran & Anil, 1999); In Brazil, imposex in Thais haemastoma New Zealand (Lepsiella scobina, Thais orbita, was first reported by Magalhães et al. (1997), in Haustrum haustorium, Xymene ambiguus, Santos Bay, São Paulo, by Fernandez et al. Taron dubius, Cominella virgata, Amalda (Ba- (1998), in Guanabara Bay, Rio de Janeiro and by ryspira) australis – Stewart et al., 1992); Aus- Castro et al. (2000), in Fortaleza, Ceará. tralia (Lepsiella vinosa – Nias et al., 1993; T. or- The present work reports recent findings on bita – Foale, 1993); Thailand (Thais distin- possible TBT related effects in two of these ar- guenda, Thais bitubercularis, Morula musiva – eas of the Brazilian coast. Bech, 1999a, 1999b; Phalium bisulcatum, Dis- torsio reticularis, Murex occa, Murex trapa, Murex tribulus, Chicoreus capucinus, Thais gra- Methodology data, Thais lacera, Babylonia areolata, Nassar- ius livescens, Nassarius stolatus, Hemifusus ter- The development of imposex in T. haemastoma natanus, Voluma conchlidium, Cymbiola no- was used as a tool to search for indications of bilis, Melo melo – Swennen et al., 1997); Indone- biological stress derived from TBT and TPT in sia (Thais kieneri, Thais savignyi, Vasum tur- Guanabara Bay and in coastal areas of Fort- binellus – Evans et al., 1995); Malaysia (T. gra- aleza. The bioindicator was selected based on data, C. capucinus, T. clavigera, Thais jubilaea, the following properties: (1) ubiquity along the T.
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